How precise is neuronal synchronization?

Recent work suggests that synchronization of neuronal activity could serve to define functionally relevant relationships between spatially distributed cortical neurons. At present, it is not known to what extent this hypothesis is compatible with the widely supported notion of coarse coding, which assumes that features of a stimulus are represented by the graded responses of a population of optimally and suboptimally activated cells. To resolve this issue we investigated the temporal relationship between responses of optimally and suboptimally stimulated neurons in area 17 of cat visual cortex. We find that optimally and suboptimally activated cells can synchronize their responses with a precision of a few milliseconds. However, there are consistent and systematic deviations of the phase relations from zero phase lag. Systematic variation of the orientation of visual stimuli shows that optimally driven neurons tend to lead over suboptimally activated cells. The observed phase lag depends linearly on the stimulus orientation and is, in addition, proportional to the difference between the preferred orientations of the recorded cells. Similar effects occur when testing the influence of the movement direction and the spatial frequency of visual stimuli. These results suggest that binding by synchrony can be used to define assemblies of neurons representing a coarse-coded stimulus. Furthermore, they allow a quantitative test of neuronal network models designed to reproduce physiological results on stimulus-specific synchronization.